Isoprene enhances leaf cytokinin metabolism and induces early senescence

Abstract

Summary Isoprene, a major biogenic volatile hydrocarbon of climate‐relevance, indisputably mitigates abiotic stresses in emitting plants. However functional relevance of constitutive isoprene emission in unstressed plants remains contested. Isoprene and cytokinins (CKs) are synthesized from a common substrate and pathway in chloroplasts. It was postulated that isoprene emission may affect CK‐metabolism. Using transgenic isoprene‐emitting (IE) Arabidopsis and isoprene nonemitting (NE) RNA‐interference grey poplars (paired with respective NE and IE genotypes), the life of individual IE and NE leaves from emergence to abscission was followed under stress‐free conditions. We monitored plant growth rate, aboveground developmental phenotype, modelled leaf photosynthetic energy status, quantified the abundance of leaf CKs, analysed Arabidopsis and poplar leaf transcriptomes by RNA‐sequencing in presence and absence of isoprene during leaf senescence. Isoprene emission by unstressed leaves enhanced the abundance of CKs (isopentenyl adenine and its precursor) by > 200%, significantly upregulated genes coding for CK‐synthesis, CK‐signalling and CK‐degradation, hastened plant development, increased chloroplast metabolic rate, altered photosynthetic energy status, induced early leaf senescence in both Arabidopsis and poplar. IE leaves senesced sooner even in decapitated poplars where source–sink relationships and hormone homeostasis were perturbed. Constitutive isoprene emission significantly accelerates CK‐led leaf and organismal development and induces early senescence independent of growth constraints. Isoprene emission provides an early‐riser evolutionary advantage and shortens lifecycle duration to assist rapid diversification in unstressed emitters.

Plant volatiles as regulators of hormone homeostasis

“…However, genetic suppression of isoprene emission in unstressed plant leaves significantly changes the carbon distribution within the MEP pathway by favouring more carotenoid synthesis (Ghirardo et al, 2014), but significantly less plastidic cytokinins (Fig. 1; Dani et al, 2021a), indicating a direct impact on in planta hormone balance. Both show that ontologies of synthesis and activity of plant isoprenoid BVOCs, hormones, and pigments are clearly under intrinsic modular metabolic constraints with an ancient evolutionary legacy (Dani et al, 2016).…”

“…Constitutive biogenic volatile organic compound (BVOC) emission often continues during senescence (Mozaffar et al, 2018;Dani et al, 2021a). If senescence is viewed as terminal metabolic stress in organs and organisms, then constitutive volatiles emitted during senescence (stress) may work analogous to stress-induced BVOCs to fortify indirect plant defense (Lin et al, 2021).…”

“…In unstressed plants, however, CKdependent cell proliferation in meristems depends on downstream mediation by NO, while NO can directly suppress CK and deactivate CK-responsive histidine phosphotransferases (Feng et al, 2013;Liu et al, 2013). By contrast, isoprene emission enhances leaf CK synthesis, CK-mediated signalling and CK degradation to induce early leaf and plant senescence (Dani et al, 2021a;Fig. 2).…”

“…SLs also promote cytokinin (CK) degradation (roots; Duan et al, 2019). Both synthesis and degradation of CKs are promoted by isoprene (leaves; Dani et al, 2021a). Isoprene and CKs suppress nitric oxide (NO) (leaves; Velikova et al, 2005;Liu et al, 2013).…”

“…pollination and defence, confers a fitness advantage to emitters over nonemitting relatives (Raguso, 2016; Kalske et al ., 2019). However, continuous induction or suppression of constitutive BVOCs in unstressed plants has significant metabolic and phenotypic consequences unrelated to stress mitigation and communication (Orlova et al ., 2006; Robert et al ., 2013; Dani et al ., 2021a). Such instances highlight unappreciated housekeeping roles for endogenous plant volatiles.…”